Avian Influenza Overview March 2023

SCIENTIFIC REPORT
APPROVED: 8 March 2023
doi: 10.2903/j.efsa.2023.7917
Avian influenza overview December 2022 – March

2023
European Food Safety Authority,
European Centre for Disease Prevention and Control,
European Union Reference Laboratory for Avian Influenza,
Cornelia Adlhoch, Alice Fusaro, José L Gonzales, Thijs Kuiken, Stefano
Marangon, Grazina Mirinaviciute, Éric Niqueux, Karl Stahl, Christoph
Staubach, Calogero Terregino, Alessandro Broglia and Francesca Baldinelli
Abstract
Between 3 December 2022 and 1 March 2023 highly pathogenic avian influenza (HPAI)
A(H5N1) virus, clade 2.3.4.4b, was reported in Europe in domestic (522) and wild (1,138)
birds over 24 countries. An unexpected number of HPAI virus detections in sea birds were
observed, mainly in gull species and particularly in black-headed gulls (large mortality
events were observed in France, Belgium, the Netherlands, and Italy). The close genetic
relationship among viruses collected from black-headed gulls suggests a southward spread
of the virus. Moreover, the genetic analyses indicate that the virus persisted in Europe in
residential wild birds during and after the summer months. Although the virus retained a
preferential binding for avian-like receptors, several mutations associated to increased
zoonotic potential were detected. The risk of HPAI virus infection for poultry due to the
virus circulating in black-headed gulls and other gull species might increase during the
coming months, as breeding bird colonies move inland with possible overlap with poultry
production areas. Worldwide, HPAI A(H5N1) virus continued to spread southward in the
Americas, from Mexico to southern Chile. The Peruvian pelican was the most frequently
reported infected species with thousands of deaths being reported. The reporting of HPAI
A(H5N1) in mammals also continued probably linked to feeding on infected wild birds. In
Peru, a mass mortality event of sea lions was observed in January and February 2023.
Since October 2022, six A(H5N1) detections in humans were reported from Cambodia (a
family cluster with 2 people, clade 2.3.2.1c), China (2, clade 2.3.4.4b), Ecuador (1, clade
2.3.4.4b), and Vietnam (1, unspecified clade), as well as two A(H5N6) human infections
from China. The risk of infection with currently circulating avian H5 influenza viruses of
clade 2.3.4.4b in Europe is assessed as low for the general population in the EU/EEA, and
low to moderate for occupationally or otherwise exposed people.
©2023 European Food Safety Authority, European Centre for Disease Prevention and
Control, European Union Reference Laboratory for Avian Influenza. EFSA Journal published
by Wiley-VCH GmbH on behalf of European Food Safety Authority
Key words: avian influenza, captive birds, HPAI, humans, monitoring, poultry, wild birds
Requestor: European Commission
Question number: EFSA-Q-2023-00094 and Commission request 280 to ECDC

(SANTE.B.2/IK/mo (2023)2182203)
Correspondence: biohaw@efsa.europa.eu and ECDC.influenza@ecdc.europa.eu
www.efsa.europa.eu/efsajournal EFSA Journal 2023;21(3):7917

Avian influenza overview December 2022 - March 2023
Acknowledgements: In addition to the listed authors, EFSA, ECDC and the EURL wish to
thank the Member State representatives who provided epidemiological data on avian
influenza outbreaks and the following Member State representatives who shared sequence
data: Sandra Revilla-Fernandeza and Irene Zimpernik (Austria), Mieke Steensels and
Steven Van Borm (Belgium), Vasiliki Christodoulou (Cyprus), Alexander Nagy (Czech
Republic), Charlotte Kristiane Hjulsager (Denmark), Béatrice Grasland, Audrey Schmitz,
François-Xavier Briand (France), Timm Harder (Germany), Laura Garza Cuartero (Ireland),
Chantal Snoeck (Luxembourg), Britt Gjerset (Norway), Krzysztof Śmietanka and Edyta
Swieton (Poland), Iuliana Onita (Romania), Nancy Beerens (the Netherlands), Monserrat
Agüero García and Azucena Sánchez (Spain), Siamak Zohari (Sweden); Claudia Bachofen
from the Institute of Virology and Immunology (Switzerland), Ian Brown from the Animal
and Plant Health Agency (United Kingdom); Camille Delavenne from AUSVET Europe for
conducting the data analysis under the contract OC/EFSA/ALPHA/2021/02; Linnea
Lindgren Kero for the support provided under the contract OC/EFSA/DATA/2021/; the
authors, originating and submitting laboratories of the sequences from GISAID’s EpiFlu™
Database, which is used for this assessment; AI-Impact, including DWHC, SOVON, and
waarneming.nl for providing monthly data on gulls found dead in the Netherlands during
the reporting period; Anne van de Wiele and Loïc Palumbo (Office Français de la
Biodiversité - French Biodiversity Agency) for information about wild bird situation;
Edoardo Colzani from ECDC as well as Inma Aznar and Gina Cioacata from EFSA for the
support provided to this scientific output.
Suggested citation: EFSA (European Food Safety Authority), ECDC (European Centre for
Disease Prevention and Control), EURL (European Reference Laboratory for Avian
Influenza), Adlhoch C, Fusaro A, Gonzales JL, Kuiken T, Marangon S, Stahl K, Niqueux É,
Staubach C, Terregino C, Mirinaviciute G, Aznar I, Broglia A and Baldinelli F, 2023. Scientific
report: Avian influenza overview December 2022–March 2023. EFSA Journal
2023;21(3):7917, 43 pp. https://doi.org/10.2903/j.efsa.2023.7917
ISSN: 1831-4732
©2023 European Food Safety Authority, European Centre for Disease Prevention and
Control, European Union Reference Laboratory for Avian Influenza. EFSA Journal published
by Wiley-VCH GmbH on behalf of European Food Safety Authority
This is an open access article under the terms of the Creative Commons Attribution-
NoDerivs Licence, which permits use and distribution in any medium, provided the original
work is properly cited and no modifications or adaptations are made.
The EFSA Journal is a publication of the European Food

Safety Authority, an agency of the European Union.
www.efsa.europa.eu/efsajournal 2 EFSA Journal 2023;21(3):7917

Table of contents
Abstract 1
1 Background 4
2 Results 4
2.1 HPAI detections in birds 4
2.1.1 HPAI detections in birds in Europe ........................................................................................... 4
2.1.2 The avian influenza situation in other countries not reporting via ADIS, 3 December
2022 to 1 March 2023 .............................................................................................................................. 13
2.2 HPAI detections in mammals 16
2.3 Genetic characterisation of avian influenza viruses 21

2.3.1 Description of the nomenclature of the HPAI A(H5) viruses used in the document21
2.3.2 Global overview of HPAI viruses of the A(H5) subtype of clade 2.3.4.4b ............... 21
2.3.3 Genetic characteristics of HPAI viruses of the A(H5N1) subtype circulating in Europe
....................................................................................................................................................... 22
2.4 Avian influenza virus infections in humans 23

2.4.1 Most recent human infections with avian influenza A(H5N1) and A(H5N6) virus 23
2.4.2 Human A(H5N1) cases, summary .......................................................................................... 24
2.4.3 Human A(H5N6) cases, summary .......................................................................................... 25
2.4.4 Details about human infections with avian influenza A(H5Nx) virus clade 2.3.4.4b
related to viruses circulating in Europe, 2021–2023 ................................................................... 26
2.4.5 Genetic characteristics of HPAI viruses of the A(H5NX) subtype from human ..... 28
2.4.6 Additional information and international risk assessments (Puryear et al., 2022)29
2.5 ECDC risk assessment for the general public in the EU/EEA 29
2.6 Options for public health response 30

3 Conclusions 32
4 Options for response 33
References 34
Annex A – Data on birds 43

1 Background
Since the latest EFSA, ECDC and EURL avian influenza overview report (EFSA et al., 2022)
published in December 2022, the epidemiological situation of avian influenza has largely
evolved. In Europe, highly pathogenic avian influenza (HPAI) cases continued to be reported
in domestic and in wild birds, particularly in gull species; the Eurasian lineage of HPAI A(H5N1)
virus introduced in the Americas continued to spread southward affecting poultry, wild bird
species and wild mammals being also associated to mass mortality events; additional avian
influenza detection were reported in humans, and mutations associated with genetic adaptation
to mammals were detected in some of the circulating viruses in mammals and also birds. This
evolving situation triggered the European Commission to request EFSA, ECDC and the EURL to
issue a targeted overview report on avian influenza considering the new epidemiological and
scientific data available.
The aim of this report is to provide technical and scientific assistance to the Commission by
providing an overview of HPAI virus detections in birds and mammals as well as human
infections due to avian influenza virus that occurred in and outside Europe between 3 December
and 1 March 2023.
2 Results
2.1 HPAI detections in birds
2.1.1 HPAI detections in birds in Europe
Figure 1 shows the HPAI outbreaks in birds that were reported in Europe via ADIS or WOAH-
WAHIS for the epidemiological years1 2016–2017, 2017–2018, 2018–2019, 2019–2020, 2020–
2021, 2021–2022 and 2022–2023 by month of suspicion. For the current epidemiological year
2022–2023 that starts on 1 October 2022, data reported are truncated on 1 March 2023.
The HPAI epidemic observed in the 2021–2022 epidemiological year was so far the largest
observed in Europe, with a total of 6,615 HPAI virus detections in 37 countries. Unexpectedly,
the epidemic continued along the summer months with an extensive spread of the virus to
colony-breeding seabirds, a group of species that were very rarely reported as HPAI affected
before (Figure 4). In July and August 2022, the HPAI virus detections in wild birds
predominantly affected the order of Suliformes (primarily northern gannets) and were reported
along the coasts, whereas from September to December 2022 waterfowl replaced colony-
breeding seabirds as the main wild birds in which most HPAI virus detection was reported
(Figure 4). As a result, there was not a clear start of the HPAI epidemic season in October in
the epidemiological year 2022–2023, neither in wild nor in domestic birds due to the
persistence of the virus in wild birds (Figure 1). In the epidemiological years 2022-2023 up to
1 March 2023, a total of 2,701 HPAI virus detections were reported, 1,649 in wild birds and
1,052 in domestic birds over 28 European countries (Table A.7).
Considering the current reporting period, from 3 December 2022 to 1 March 2023, 1,660 HPAI
virus detections were reported in poultry (403), captive (119) and wild birds (1,138) (Figure
2, Table A.7).
HPAI outbreaks in poultry were reported in France (191), Poland (88), Hungary (31), Czechia
(26), Germany (20), United Kingdom (19), Belgium (6), Austria (3), Denmark (3), the
Netherlands (3), Romania (3), Slovakia (3), Italy (2), Spain (2), Bulgaria (1), Moldova (1),
Slovenia (1) (Figure 2, Table B1). Out of those 403 outbreaks, 78 were reported to be
secondary outbreaks in France (33/191), Hungary (27/31), Poland (14/88), Romania (2/3),
Belgium (1/6), Czechia (1/26). In the current reporting period, the number of poultry outbreaks
1 In this document an ‘epidemiological year’ refers to the period starting on week 40 (the beginning of October) and
ending on week 39 (the end of September) of the following year, based on the dates on which the first HPAI virus
detections were observed in wild birds in Europe in 2016–2017, 2020–2021 and 2021–2022.

continued to decrease from its higher point in November 2022 (Figure 3). Poultry outbreaks in
France concentrated in Pays-de-la- Loire during the first half of the reporting period (124/191)
and occurred primarily in domestic duck. With the exception of Hungary, most outbreaks have
not been attributed to secondary spread. The most likely source of infection reported by
countries seems to be indirect contact with wild birds or unknown. The information on the
poultry species affected in the outbreaks were collected too close to the publication of the
presents report, therefore these aspects will be analysed and fully described in the following
EFSA, ECDC, EURL scientific report.
HPAI detections in captive birds were reported in Germany (52), France (27), United Kingdom
(15), Belgium (11), Austria (4), the Netherlands (4), Hungary (1), Luxemburg (1), Poland (1),
Slovakia (1), Slovenia (1) and Sweden (1) (Figure 2, Table B1). Out of those 119 outbreaks in
captive birds 28 were reported as secondary outbreaks in Germany (27) and France (1).
During this reporting period, the vast majority of the wild bird detections were reported in sea
birds, particularly in Laridae species, with the black-headed gull being the most affected gull
species, followed by the herring gull (Figure 4).
In the period 3 December 2022 to 1 March 2023, there was a peak of HPAI virus detections in
wild birds and poultry in January 2023 that was about one-third lower than that in January
2022, but slightly higher than in January 2021 (Figure 1). On wild birds, the number of HPAI
virus detections in wild birds in the January 2023 peak was similar to that in January 2022 with
an important difference: in the January 2023 peak, nearly all the wild birds were in the category
‘colony-breeding seabirds’, compared to mainly waterbirds in the January 2022 peak (Figure
4a). Within the category ‘colony-breeding seabirds’, nearly all wild birds found infected in
January 2023 belonged to the family Laridae (gulls, terns and skimmers) and were
predominantly black-headed gulls (Chroicocephalus ridibundus or Larus ridibundus), with fewer
European herring gulls (Larus argentatus) (Figure 4b and 4c). The complete list of wild bird
species found as HPAI virus infected from 3 December 2022 to 1 March 2023 is reported in
Figure A.1 in Annex A. In January 2023, the weekly reported HPAI virus detections in black-
headed gulls ranged from 14 to 50, which is substantially higher than that in the period October
2020 to December 2022 (1 to 8) (Figure 4c).
Those HPAI virus detections concentrated inland in Belgium, France, the Netherlands,
Germany, Austria, Italy, northern Spain and increased from the end of January 2023 (Figures
5 and 6). The geographical distribution of HPAI virus detections between wild bird categories
differed in this period. HPAI virus detections in waterbirds (mainly swans, geese, and mallards)
were reported mainly from northern and eastern Europe, and those in seabirds (mainly black-
headed gulls) mainly from southern and western Europe (Figures 5 and 6). It remains to be
seen whether this pattern will change as black-headed gulls move north during spring migration
and return to their breeding colony sites.
During this reporting period, mortality events affecting different wild bird species, particularly
gull species, were observed in several countries. In France, during January 2023, increased
mortality of wild birds was reported in the Île-de-France and Centre-Val-de-Loire regions
around Paris: close to Chartres (Eure-et-Loir), 150 carcasses of gulls were found on a pontoon
of a private pond (Franceinfo, online). Several other hotspots of abnormal black-headed gull
mortality were also reported, accounting for over 1,900 dead birds in Essonne and Seine-et-
Marne (close to Paris) during January and early February 2023, more than 100 dead birds in
Moselle and Meurthe-et-Moselle (eastern France, close to Luxembourg and Germany) during
the last week of January 2023, and around 50 dead birds in Maine-et-Loire (western France)
in February 2023. Carcasses of a few bird-eating raptors, subsequently confirmed as being
infected with A(H5N1) HPAI virus, were also found in some of these hotspots (Personal
communication: LoÎc Palumbo and Anne van de Wiele, Office Français de la Biodiversité). In
Belgium, in the second half of February 2023, increased numbers of carcasses of black-headed
gulls, that had died from HPAI, were found washed ashore along the river Meuse in the province
of Limburg, Belgium (nws, online). In the Netherlands, on 12 February 2023, a wild bird
rehabilitation centre in Rotterdam reported increased numbers of black-headed gulls with

neurological signs in the area, confirmed to be due to HPAI in recent weeks (Vogelklas, online).
On 20 February, 30 dead black-headed gulls were found dead due to HPAI in a grassland area
managed for meadowbirds ‘Landje van Geijsel’ bij Ouderkerk, the Netherlands (Trouw, online).
On 3 March, 33 dead black-headed gulls were reported from a roosting site in Veenoordskolk,
Deventer municipality, the Netherlands 2. On 3 March, Dutch animal ambulance personnel
reported high numbers of dead and sick black-headed gulls, including with neurological signs,
in the areas around Weert, Den Bosch, Schaijk, Eindhoven, and Eersel 3 In northern Italy,
mainly in the area of the Garda lake, an unprecedented increase in mortality in black-headed
gulls was observed in the first months of 2023. Hundreds of animals were found dead or
seriously ill (Brescia oggi, online). The exact number of gulls involved in these events is not
known because in many cases the carcasses were eliminated by the competent authorities
without being counted and/or sent to diagnostic laboratories. The characterised viruses from
more than 50 birds tested since the beginning of February were all closely related and belong
to the clade 2.3.4.4b, genotype H5N1-A/Herring_gull/France/22P015977/2022-like. Events of
mortality in gulls was also reported in Switzerland, Diagnostic tests on these samples are
ongoing.
Additional data available for the Netherlands from AI-Impact, DWHC, SOVON, and
waarneming.nl on gull mortality observed monthly from December to February in the
epidemiological years 2021-2022 and 2022-2023 reported a markable increase in the mortality
of black headed gulls in February 2023 compared to the previous year (Table A.1).
The black-headed gull breeds across Europe and Asia between the latitudes of about 40 and
70 degrees north, with small breeding populations in Iceland, Greenland and the east coast of
North America. Within this breeding range, northern populations are migratory, and
populations further south are partially migratory, with a wintering range extending to Africa
and southern Asia up to about the equator, mainly along the coast. The global population of
black-headed gulls is about 2 to 3 million breeding pairs.
The European wintering population of black-headed gulls is over 4 million birds. Inland
wintering, associated with human activities, has increased since 1960. Spring migration in
Central Europe starts in early February and peaks in late March-early April for adults, with less
pronounced migration of first-year birds into mid-May. Breeding sites are occupied in March.
There are often large flocks in areas around breeding sites before re-occupation. Departure
from breeding sites starts from early July, with dispersal of first-year birds in different
directions. Autumn migration in Europe starts around late May and extends to early January,
depending on latitude and age category (in sequence of timing: immatures, non-breeding
adults, breeding adults and juveniles).
Black-headed gulls breed in dense colonies often of several thousands, but rarely >10,000
pairs, mostly in lakes surrounded by reedbeds with small islands; also coastal sand islands,
bogs, and artificial ponds. In Europe, black-headed gulls breed in most countries, with higher
numbers in the north. Historical capture-recapture data from ringing activities from EURING4
and real time bird distribution data by EuroBird Portal5 on the expected movements of black
gulls in the coming weeks/months indicate a general east and north east movement from places
where the H5N1 virus has been detected in this species (France, Belgium, the Netherlands,
Italy), with large numbers still being observed particularly in Belgium and the Netherlands in
the next months (Tables A.2 – A.5). Those data can be consulted in the Migration Mapping Tool
developed by EFSA, EURING, Euro Bird Portal available online6.
Although categorized under 'colony-breeding seabirds’ in EFSA reports, black-headed gulls

occur both along sea coasts and inland. They feed in open areas such as farmland and towns,
2
https://twitter.com/ErikMensonides/status/1631640351550107648?s=20
3
https://twitter.com/MariskaKolk/status/1631734895557898240?s=20
4
https://euring.org/data-and-codes/euring-databank
5
https://eurobirdportal.org/ebp/en/#home/HIRRUS/r52weeks/CUCCAN/r52weeks/
6
https://euring.org/research/migration-mapping

and are abundant near human settlements. In towns and garbage dumps they feed on refuse,
and elsewhere on crabs, fish, earthworms and insects.
*When the date of suspicion is not available then the date of confirmation is used to assign the week of suspicion.
United Kingdom data are from ADNS up to 31 December 2020. From 1 January 2021 onwards, the data source was
the World Animal Health Information System (WOAH-WAHIS) for United Kingdom (excluding Northern Ireland), and
ADNS/ADIS for the United Kingdom (Northern Ireland)7.
Source: ADIS and WOAH (data extraction carried out on 1 March 2023).
Figure 1: Distribution of the number of HPAI virus detections in domestic and wild
birds reported in Europe in the epidemiological years 2016–2017, 2017–2018,
2018–2019, 2019–2020, 2020–2021, and 2021-2022 by month of suspicion,
from 1 October 2016 to 10 March 2023 (16,408)
7
In accordance with the Agreement on the Withdrawal of the United Kingdom from the EU, and in particular with the
Protocol on IE/NI, the EU requirements on data sampling are also applicable to the United Kingdom (Northern
Ireland).

Disclaimer: The designations employed and the presentation of material on this map do not imply the expression of
any opinion whatsoever on the part of the European Food Safety Authority concerning the legal status of any
country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries.
* This designation is without prejudice to positions on status, and is in line with United Nations Security Council
Resolution 1244 and the International Court of Justice Opinion on the Kosovo Declaration of Independence.
ADNS/ADIS for United Kingdom (Northern Ireland)7.
Source: EFSA, ADIS and WOAH (data extraction carried out on 1 March 2023).
Figure 2: Geographical distribution, based on available geocoordinates, of highly

pathogenic avian influenza virus outbreaks in poultry and captive birds (522)
reported by virus subtype in Europe from 3 December 2022 to 1 March 2023

Source: EFSA, ADIS and WOAH (data extraction carried out on 1 March 2023).
* When the date of suspicion is not available then the date of confirmation is used to assign the week of suspicion.
** ‘Other’ groups all other affected countries that are not indicated in the legend
*** The information on poultry species affected from middle of November 2022 were collected too close to the
publication of this report to be here analysed and reported; therefore, it will be fully described in the next EFSA,
ECDC, EURL scientific report.
Figure 3: Distribution of the highly pathogenic avian influenza virus detections in

poultry (522) in Europe by week of suspicion, from October 2020 to 1 March
2023

*When the date of suspicion is not available then the date of confirmation is used to assign the week of suspicion.
**‘Other wild species’ category contains unknown bird species, or categories different from those displayed. The
complete list of species by each wild bird category is reported in Table A.8 in Annex A.
Source: ADNS, ADIS and WOAH (data extraction carried out on 1 March 2023), EFSA.
Note that the scale of the vertical axes is specific to each category and that the unit reported is the number of HPAI
detections in different wild bird species and not the number of HPAI detections in wild birds (as more than one
species can be involved in one single HPAI reported detection).
Figure 4: Distribution of total number of HPAI virus detections reported in Europe

by week of suspicion (dates indicate the first day of the week) and (a) affected
wild bird categories (8,216), (b) affected colony-breeding seabird families
(1,751), (c) affected Laridae species (1,274), from October 2020 to 1 March
2023

* This designation is without prejudice to positions on status, and is in line with United Nations Security Council
Resolution 1244 and the International Court of Justice Opinion on the Kosovo Declaration of Independence.
Source: EFSA, ADIS and WOAH (data extraction carried out on 1 March 2023). Note that in one single detection
more than one wild bird species might be involved and each wild bird categories detected as HPAI infected is
presented in the map.

pathogenic avian influenza detections in wild birds’ categories in Europe, by
species category, from 3 December 2022 to 1 March 2023


Source: ADIS and WOAH (data extraction carried out on 1 March 2023). Note that in one single detection more than
one wild bird species might be involved and each wild bird categories detected as HPAI infected is presented in the
map

pathogenic avian influenza detections in gull species in Europe at bi-weekly
intervals, from 3 December 2022 to 1 March 2023
2.1.2 The avian influenza situation in other countries not reporting via
ADIS, 3 December 2022 to 1 March 2023
An overview of the HPAI virus detections in birds notified from other countries not reporting
via ADIS but via the WOAH from 3 December 2022 to 1 March 2023 is presented in Table 1
and Figure 7. Please note that the actual situation in South America is continuing evolving
with new HPAI virus detections in wild, domestic birds and mammal species being reported to
the public via different means, e.g. this is the case of more poultry outbreaks than those
displayed in Table 1 reported by Argentina on 6 March 2023 (SENASA, 2023). However, in
the tables and figures of the current report only the data extracted from WOAH on 1 March
are presented; information available from other sources has not been systematically
retrieved and is only described in the text.
Since its introduction in Central/South America in October 2022, HPAI A(H5N1) rapidly spread
across South America. Worldwide, HPAI A(H5) virus continued to be detected in poultry during
the current reporting period with a comparable level of reported outbreaks as in the previous
reporting period from 10 September to 2 December 2022 (EFSA et al., 2022b). The number of
notifications increased in Asia by approximately four times (55 vs 195) and three more
countries (Kazakhstan, Nepal, Philippines and Turkey) have been reporting outbreaks to WOAH.
Canada and the USA reported the vast majority of outbreaks from the Americas, with the
reported number of outbreaks slightly more than halved compared to the previous reporting
period. However, HPAI A(H5N1) virus has continued to spread in Central and South America,
doubling the number of countries affected since the last report (6 vs 13). Since 3 December
2022, HPAI A(H5) virus has also been detected on poultry farms of different sizes in Argentina,
Bolivia, Chile, Costa Rica, Honduras, Panama, Peru and Uruguay; Cuba reported an HPAI virus
outbreak in a zoo
The list of wild bird species that have been reported to WOAH WAHIS as HPAI infected from
South America since 3 December 2022 is presented in Table A.6. Additional information about
HPAI virus detections in wild birds, not reported in WAHIS, was retrieved from different media
sources and is reported below.
In Central America (Guatemala, Honduras, El Salvador, Nicaragua, Costa Rica, Panama),

mortality of brown pelicans (Pelecanus occidentalis) was reported in association with HPAI
A(H5N1) virus detections in Panama (25 December, 1 dead), Honduras (5 January, 41 dead),
Costa Rica (25 January, 3 dead, as well as 1 peregrine falcon), and Guatemala (14 February,
unknown number). On 7 February, HPAI A(H5N1) also was reported in captive wild birds
belonging to the Zoological Garden of Havana, Cuba.
Along the Pacific coast of South America (Colombia, Ecuador, Peru, Chile), corresponding to
the Pacific Americas flyway and partially separated from the rest of South America by the
physical barrier of the Andes Mountains, there was extensive mortality of wild birds and wild
mammals associated to HPAI A(H5N1) virus detections in the reporting period. The first report
was a mortality event of 200 Peruvian pelicans (Pelecanus thagus) in Peru due to HPAI A(H5N1)
on 10 November 2022. The infection spread rapidly, and by the end of 2022 over 50,000
seabirds along the coast of Peru were reported dead, including 16,890 Peruvian pelicans
(endangered in Peru), 4,324 brown boobies (Sula leucogaster) (endangered in Peru), 630 blue-
footed boobies (Sula nebouxii), 168 guanay cormorants (Leucocarbo bougainvillii) (near
threatened in Peru) (Gamarra-Toledo et al., 2023). In addition, the virus spread to marine

mammals in Peru, with 634 South American sea lions (Otaria flavescens), 4 South American
fur seals (Arctocephalus australis) and a dolphin (Tursiops truncates) according to Gamarra-
Toledo et al. (2023) or Delphinus delphis according to Leguia et al. (2023) reported dead on
Peruvian coasts during January and the first days of February 2023 in association to HPAI
A(H5N1) virus detections (Gamarra-Toledo et al., 2023). On 4 March, the agriculture ministry
reported at least 3,487 South American sea lions had been found dead in Peru in association
with the HPAI A(H5N1) outbreak. This represents about 3.3% of the total population in the
country8.
Southwards from Peru, HPAI A(H5N1) virus was first reported in Peruvian pelicans in the
administrative regions of Tarapacá and Antofagasta, northern Chile at a latitude of about 20
degrees South, on 8 December 2022. By 13 February 2023, it had reached southwards to
Ancud in Los Lagos, the third southernmost administrative region of Chile at about 42 degrees
South, where HPAI A(H5N1) was detected in a kelp gull (Larus dominicanus). By 1 January
2023, 3,247 wild seabirds killed by the virus between Arica and Valparaíso had been buried,
but the actual mortality was undoubtedly many times higher. The virus was detected in many
wild bird species in Chile (Table A.6); those with high mortality included Peruvian pelicans, kelp
gulls, Belcher's gulls (Larus belcheri), gray gulls (Leucophaeus modestus), guanay cormorants,
Peruvian boobies, elegant terns (Thalasseus elegans), and turkey vultures (Cathartes aura). In
addition, HPAI A(H5N1) virus was detected in two South American sea lions along the Chilean
coast, both in the administrative region Antofagasta. On 7 March, a marine otter (Lontra felina)
in Arica, Chile, was reported infected with HPAI (H5N1) virus (El Diario de la Araicania,
online).On the east side of the Andes Mountains (Ecuador, Colombia, Venezuela, Guyana,
Surinam, French Guiana, Brazil, Bolivia, Paraguay, Uruguay, Argentina), there was far less
mortality of wild birds compared to the west side, and none of wild mammals, reported in the
period 3 December 2022 to 1 March 2023. The highest reported wildlife mortality was a die-off
of 172 Peruvian pelicans from HPAI A(H5N1) on the coast of Venezuela, reported on 10
December 2022. This location corresponds both with the Mississippi and the Atlantic Americas
Flyways.
Although HPAI A(H5N1) virus in poultry was reported in Colombia, there were no reported
detections in wild birds. HPAI A(H5N1) virus was reported in blue-and-white swallow
(Pygochelidon cyanoleuca) in Bolivia (nearby an affected poultry farm), and in 5 black-necked
swans (Cygnus melancoryphus) on the coast of Uruguay on 16 February 2023. The black-
necked swan is resident in Argentina, Brazil, Chile, Uruguay, and the Falkland Islands, not a
migratory species from further north. Therefore, the black-necked swan cases in coastal
Uruguay suggest that HPAI A(H5N1) virus may have spread south with wild bird migration
along the Atlantic Americas Flyway.
HPAI A(H5N1) virus was reported in Andean geese (Chloephaga melanoptera) in Jujuy,
Argentina, on 16 February 2023, and in a red-gartered coot (Fulica armillata) in Neuquén,
Argentina, on 22 February 2023. At a latitude of about 40 degrees South, this is the furthest
south that HPAI A(H5N1) virus detection has been reported east of the Andes Mountains. Since
both Jujuy and Neuquén are located on the eastern slope of the Andean Mountains, bordering
Chile, it cannot be excluded that virus incursion came across the mountains from Chile, where
the virus already was present.
There were very few HPAI virus detections reported from African countries (e.g. Egypt) and
China to WOAH WAHIS, although some HPAI viral sequences from birds have been deposited
in GISAID. The very scarce information available raise uncertainty about possible circulation of
HPAI virus in those areas.
8
https://twitter.com/BNOFeed/status/1631491427413680128

Table 1: Number of HPAI virus detections in non-European countries, by virus subtype

and country, from 3 December to 1 March 2023
Domestic birds Wild birds

Region Country A(Not A(Not Total
A(H5N1) A(H5N2) A(H5N5) A(H5Nx) A(H5N1) A(H5Nx)
typed) typed)
Niger 2 2
Africa (6) Nigeria 3 3
South Africa 1 1
Argentina 2 2 4
Bolivia 15 1 16
Canada 17 1 18
Chile 1 53 54
Colombia 9 9
Costa Rica 1 5 6
Cuba 1 1
Americas Ecuador 13 2 15
(265) Guatemala 1 1
Honduras 3 3
Mexico 8 8
Panama 2 5 7
Peru 13 3 16
United States
89 17 106
of America
Uruguay 1 1
Taiwan 26 8 1 35
Hong Kong 1 1
India 10 10
Israel 9 2 11
Asia Japan 52 1 39 8 100
(195) Kazakhstan 1 1
Korea 25 25
Nepal 7 7
Philippines 3 3
Turkey 2 2
Europe
Russia 4 1 5
(5)
Total 299 9 1 14 2 123 18 5 471
Source: WOAH-WAHIS (data extraction carried out on 1 March 2023).


pathogenic avian influenza virus detections reported in domestic birds (847) and
wild birds (1,284) by virus type, from 3 December 2022 to 1 March 2023
2.2 HPAI detections in mammals

During the period from 3 December 2022 to 1 March 2023, HPAI A(H5N1) viruses were reported
in several mammal species in Europe and Americas: in cats and red foxes in France and the
USA, in ferrets in Belgium, in lynx, skunk, raccoon, mountain lion, brown bear and American
black bear in USA and in sea lions in Peru and in Chile (Table 2).
The geographical distribution of HPAI A(H5) viruses, clade 2.3.4.4b, that have been reported
since October 2020 are presented in Figure 8. These reports involve 24 species of carnivores,
4 species of cetaceans, as well as domestic pigs and wild boar (artiodactyls) and Virginia
opossums (marsupials). The mammal species involved are mainly those that hunt wild birds,
feed on dead wild birds, or both. The species in which HPAI A(H5N1) virus was reported most
frequently is the red fox, which lives all across Europe, north Africa, most of Asia apart from
the extreme southeast, and North America except southwest USA and Mexico (GBIF, online;
IUCN, online). The frequent detection of HPAI A(H5N1) virus in red foxes is likely a consequence
of its wide distribution, which largely overlaps the geographical spread of the HPAI A(H5N1)
outbreaks, and its diet, which partly includes both hunted and scavenged wild birds.
While most of the reports of HPAI (H5N1) virus in mammals consist of single or at most a few
animals, there were three mass mortality events of mammals associated with HPAI A(H5N1)
virus detections in 2022 (USA and Spain) and 2023 (Peru) and possible mammal-to-mammal
transmission (Figure 8). The first was an unusual mortality event of seals, including harbour
seals, on the coast of Maine, USA, in the summer of 2022, which coincided with an outbreak
of HPAI A(H5N1) virus in wild birds in the region (Puryear et al., 2022). The majority of stranded
seals were found dead. Of those that stranded live, symptoms included respiratory signs with
a subset of neurologic cases. Of the seals examined between 21 June and 13 July, a total of 15

of 25 harbour seals and 2 of 4 grey seals tested positive for HPAI A(H5N1) virus (details of
genetics in section 2.3.3). The source of the virus was likely infected wild birds. However, the
authors of the preprint report considered it unlikely that multiple seals acquired virus through
predation or scavenging of an infected source, as birds are not a typical food source for harbour
or grey seals. Instead, transmission likely occurred through either environmental transmission
or direct contact between seals, though the data did not allow to distinguish between these
two possible routes.
The second involved a farm of 52,000 American minks, housed in 30 partially open barns in
Galícia, northwest Spain (Aguero et al., 2023). These animals showed an increased mortality
rate in the first week of October 2022 (0.8% vs 0.2%). Mortality peaked at 4.3% (>2,200
mink) in mid-October. Clinical signs of infection in minks included loss of appetite,
hypersalivation, depression, bloody snout and neurological manifestations such as ataxia and
tremors. Out of 15 minks tested, 14 were positive for HPAI A(H5N1) virus (details on genetics
in section 2.3.3). The feed of the minks included raw poultry by-products, but there had been
no HPAI A(H5N1) virus outbreaks in the region from where these by-products were obtained,
whereas several HPAI A(H5N1) cases in yellow-legged gulls and northern gannets were
detected in that region. Given that the open housing system of mink farming is known to allow
the access to wildlife including wild birds into the farms, and that direct contact with mink is
possible (European Food Safety et al., 2021; Sikkema et al., 2022), the mink may have been
in contact with infected wild birds that were attracted to the mink feed. However, it is difficult
to explain all the infections of mink by bird-to-mink contact. Instead, the authors of the report
state that their findings indicate onward transmission to other mink, based on increasing
number of infected animals and progression of the infection from the initially affected area to
the entire holding.
The third HPAI A(H5N1) outbreak in mammals involved two species of sea lions in Peru
(Gamarra-Toledo et al., 2023). This sea lion die-off coincided with an outbreak of HPAI A(H5N1)
in seabirds in Peru, associated with the mortality of >50,000 birds by the end of 2022,
particularly Peruvian pelicans and Peruvian boobies. In the first 5 weeks of 2023, 630 South
American sea lions and 4 South American fur seals were found dead on the coast of Peru, with
up to 100 carcasses floating together at sea. The clinical symptoms of dying individuals were
mainly neurological, such as tremors, convulsions and paralysis. They also showed respiratory
signs such as dyspnea, tachypnea, nasal and buccal secretions and pulmonary edema. Of 12
sea lions tested, 9 were positive for HPAI A(H5N1) (details on genetics below). The source of
the virus affecting these sea lions was very probably the large number of infected birds on the
Peruvian coastline. Sea lions may have been infected by close contact or consumption of these
birds or their carcasses. However, since many animals died simultaneously in groups, the
authors could not exclude direct transmission among sea lions due to their colonial breeding,
and because.

Avian influenza overview December 2022 – March 2023
Disclaimer: The designations employed and the presentation of material on this map do not imply the expression of any opinion whatsoever on the part of the European Food Safety Authority
concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries.
Figure 8: Geographical distribution of detections of HPAI in mammals since 2016 (based on Table 2)

Table 2: Avian influenza A(H5Nx) virus detections in mammal species other than humans related to circulating viruses worldwide, 2016–2022
Virus Animal (order, family, species) Epidemic

Country Reference
season
Artiodactyla Suidae Domestic pigs (Sus scrofa), serological December
A(H5N8) clade 2.3.4.4b
France (Herve et al., 2021)

detection 2016
Wild boar, serological detection Germany 2017 (Schülein et al., 2021)
Carnivora Phocidae Poland, United November (Shin et al., 2019; Floyd et al., 2021;
Grey seals (Halichoerus grypus) Kingdom, 2016; SVA, online-b); personal communication
Sweden 2020-2021 by Siamak Zohari, SVA)
Germany, United (Floyd et al., 2021; Ärzteblatt, online;
December
Harbour seals (Phoca vitulina) Kingdom; Avian Flu Diary, online-b; Outbreak News,
2020
Denmark online; SSI, online)
Canidae December
Red foxes (Vulpes vulpes) United Kingdom, (Floyd et al., 2021)
2020
Carnivora Canidae Sweden;
Netherlands; (SVA, online-b; WOAH, online-a, b;USDA,
Finland; France, 2020-2021 online); personal communication by
Red foxes (Vulpes vulpes) Estonia; Ireland; 2021-2022 Siamak Zohari, SVA; Irish National
Belgium; 2022-2023 Reference Laboratory for Avian Influenza,
Norway; Japan; personal communication)
USA; Canada
Common raccoon dog (Nyctereutes
Japan 2021-2022 (WOAH, online-b)
procyonoides)
Coyote (Canis latrans) USA 2021-2022 (WOAH, online-b)
Mustelidae Netherlands;
Eurasian otter (Lutra lutra) 2021-2022 (WUR, online)
Finland
European badger (Meles meles) Netherlands 2021-2022 (WUR, online)
European polecat (Mustela putorius) Netherlands 2021-2022 (WUR, online)
(Slovenian National Reference Laboratory
2021-2022 for Avian Influenza, personal
A(H5N1) clade 2.3.4.4b
Ferret (Mustela furo) Slovenia, Belgium

2022-2023 communication; European Commission,
online)
2021-2022
American mink (Neovison vison) Canada, Spain (Galicia, online; WOAH, online-b)
2022-2023
Felidae Lynx (Lynx lynx) Finland 2021-2022 (FFA, online)
2021-2022
Bobcat (Lynx rufus) USA (WOAH, online-b)
2022-2023
Fisher cat (Pekania pennanti) USA 2021-2022 (WOAH, online-b)
Amur leopard (Panthera pardus) USA 2021-2022 (USDA, online)
Amur tiger (Panthera tigris)(b) USA 2022-2023 (WOAH, online-b)

Mountain lion (Puma concolor) USA 2022-2023 (WOAH, online-b)

Cat (Felis catus) France, USA 2022-2023 (WOAH, online-b)
Procyonidae 2021-2022
Raccoon (Procyon lotor) USA (WOAH, online-b)
2022-2023
Mephitidae 2021-
(CTV News, online; USDA, online; WOAH,
Skunks (Mephitis mephitis) Canada; USA 2022;
online-b)
2022-2023
Otaridae (Gamarra-Toledo et al., 2023; WOAH,
South American sea lion (Otaria flavescens) Peru;Chile 2022-2023
online-b)ref
Phocidae 2021-2022 (AMMI, 2022; Agriland, online; WOAH,
Grey seals (Halichoerus grypus) USA; Canada; UK
2022-2023 online-b)
2021-2022
Harbour seals (Phoca vitulina) USA; Canada; UK (Agriland, online; WOAH, online-b)
2022-2023
Ursidae Canada 2021-2022 (Healthy Wildlife, online; KTOO, online;
American black bear (Ursus americanus)
USA 2022-2023 WOAH, online-b)
Brown bear (Ursus arctos) USA 2022-2023 (Kiniradio, online; USDA, online)
Artiodactyla Suidae Domestic pigs (Sus scrofa), serological
Italy 2021-2022 EURL
detectiona
Didelphimorphia Dedelphidae 2021-2022
Virginia opossum (Didelphis virginiana) USA (USDA, online; WOAH, online-b)
2022-2023
Cetacea Phocoenidae Porpoise (Phocoena phocoena) Sweden 2021-2022 (SVA, online-a)
Delphinidae Bottlenose dolphin (Tursiops truncatus) USA 2021-2022 (UFHealth, online; WOAH, online-b)
White-sided dolphin (Lagenorhynchus acutus) Canada 2022-2023 (Avian Flu Diary, online-a)
Common dolphin (Delphinus delphi) Peru 2022-2023 (Leguia et al., 2023)
(a) Serological detection in a HPAI outbreak in a backyard poultry
(b) Captive bird into a zoo

2.3 Genetic characterisation of avian influenza viruses

2.3.1 Description of the nomenclature of the HPAI A(H5) viruses
used in the document
The HA gene of clade 2.3.4.4 A(H5) viruses has rapidly evolved since the most recent
official update of the nomenclature of the A/goose/Guangdong/1/1996-lineage H5Nx virus
(Smith et al., 2015). This clade emerged in China in 2008 and since then it has acquired
various neuraminidase subtypes, including N1, N2, N3, N4, N5, N6 and N8, by
reassortments with other avian influenza viruses from different regions, and has evolved
into several subgroups. While a revised nomenclature of clade 2.3.4.4 viruses is pending,
in previous reports we used the genetic clustering described in 2018 by Lee and co-authors,
who recognised four groups (a–d) within clade 2.3.4.4 (Lee et al., 2018). Recently, an
update to the unified nomenclature for clade 2.3.4.4 A(H5) viruses has been proposed by
the WHO (WHO, 2020) and eight genetic groups (a–h) have been recognised. To align the
nomenclature system between international organisations this classification has been
adopted for this report. Based on this proposed clustering, A(H5) viruses of clades 2.3.4.4a
and d–h have mainly been circulating in poultry in Asia, while clades 2.3.4.4b and 2.3.4.4c
have spread globally through wild bird migrations during 2014–2015 (2.3.4.4c) and from
2016 to the present day (2.3.4.4b). A list with the distribution of the different genetic
clades reported by countries globally from birds, humans and the environment has been
published by WHO in February 2023 (WHO, 2023).
2.3.2 Global overview of HPAI viruses of the A(H5) subtype of clade

2.3.4.4b
Since their first identification in late 2020 in Northern Europe, A(H5N1) viruses of clade
2.3.4.4b have spread globally, reaching even countries where the HPAI (H5) viruses of the
Gs/GD lineage had never been found, and undergoing multiple reassortment events. In
January 2021, an A(H5N1) related to the 2020–2021 European viruses was reported in
West Africa (Lo et al., 2022) and subsequently in South and North African countries (Makalo
et al., 2022; El-Shesheny et al., 2023). Since then, this virus has been persistently
circulating in this geographic areas, and in West Africa it reassorted with the A(H9N2)
subtype of the zoonotic G1 lineage (Ouoba et al., 2022). From late 2021, clade 2.3.4.4b
A(H5N1) viruses, some of them closely related to the ones previously identified in Europe,
have been detected in South and East Asia (Cui et al., 2022). In December 2021, A(H5N1)
viruses of clade 2.3.4.4b, strongly related to the A(H5N1) identified in Northern Europe
during the 2020-2021 epidemiological year, were introduced from the Atlantic flyway in
North America (Bevins et al., 2022; Caliendo et al., 2022). This was followed, at the
beginning of 2022, by a second introduction from the Pacific flyway of an A(H5N1) virus
related to the ones circulating in Japan (Alkie et al., 2022). Since then the virus has spread
all over North America further evolving through reassortment events with LPAI viruses of
the American lineages (Alkie et al., 2022). In October 2022, the A(H5N1) was identified
for the first time in Mexico and soon after in Central and South America, where the virus
affected twelve countries causing episodes of mass mortality events in wild birds and in
sea lions (BBC, online; KFGO, online). The characterized viruses from South America are
related to the A(H5N1) circulating in North America (ProMed, online) and have been
described as reassortant between the Eurasian and American lineages (WOAH, 2022).
Based on the limited genetic information available to date on the viruses collected from
mammals (one dolphin and one sea lion), no mutation associated to mammalian host
adaptation has been observed (Leguia et al., 2023).

2.3.3 Genetic characteristics of HPAI viruses of the A(H5N1) subtype

circulating in Europe
Genetic diversity of A(H5N1) viruses in avian species
Since October 2020, 6 subtypes (A(H5N1), A(H5N2), A(H5N3), A(H5N4), A(H5N5),

A(H5N8)) and more than 60 different genotypes have been identified in Europe. While the
2020-2021 epidemiological year was dominated by the H5N8-A/Duck/Chelyabinsk/1207-
1/2020-like genotype, the 2021–2022 epidemiological year was mainly driven by three
H5N1 genotypes, H5N1-A/Eurasian_Wigeon/Netherlands/1/2020-like, H5N1-
A/duck/Saratov/29-02/2021-like and H5N1-A/Herring_gull/France/22P015977/2022-like.
Differently from the previous epidemics in Europe and based on the available genetic data,
no new virus incursions seem to have occurred in Europe during the 2022-2023
epidemiological year. Since October 2022, 16 distinct genotypes have been identified
among the characterized viruses. Four of them have been circulating from the 2021-2022
epidemiological year, while the remaining 12 genotypes have newly emerged very likely
from reassortment events with AIVs circulating in Eurasian wild bird populations. The
majority of the characterized viruses belong to genotype H5N1-A/duck/Saratov/29-
02/2021-like, which has been the most prevalent since the beginning of 2022. However,
starting from December 2022, a rapid increase in the number of detections of the H5N1
A/Herring_gull/France/22P015977/2022-like genotype has been recorded.
Genotype H5N1 A/Herring_gull/France/22P015977/2022-like had emerged through

reassortment events with the gull-adapted H13 subtype. It was identified for the first time
in May 2022 in France and since then it has been extensively circulating mainly in sea birds
in Northern Europe (France, The Netherland and Belgium) throughout the summer months,
with the European herring gull representing the most affected species based on the
analysed sequences. In October 2022, this genotype was also identified in Ireland and
Spain. From December 2022, we have assisted to a rapid escalation in the number of
detections of the H5N1 A/Herring_gull/France/22P015977/2022-like genotype, associated
to the increase in the number of cases in black-headed gulls, mainly in Belgium, France
and for the first time also in northern Italy.
Besides sea birds, this genotype has sporadically infected also wild anseriformes, raptors,
domestic birds (chicken, turkey and duck), at least 2 in Belgium, 2 in Ireland and 1 in
France, and mammals, including a red fox in Belgium and domestic minks reared for fur in
Spain (Aguero et al., 2023).
Mutations identified in A(H5N1) viruses from avian species
Molecular analyses of the A(H5N1) viruses circulating in birds in Europe during the 2022–
2023 epidemiological year indicate that these viruses continue to be well-adapted to avian
species, as they retain a preferential binding for avian-like receptors. However, several
mutations previously described in the literature (Suttie et al., 2019) to i) enhance
polymerase activity and replication in mammals or mammalian cells, ii) increase virulence,
iii) increase/confer resistance toward antiviral drugs, iv) in vitro increase binding to human-
type receptors alpha2,6-SA, and v) decrease antiviral response in ferrets were observed
with a frequency varying for the distinct mutations. The real effect of these mutations on
the biological characteristics of the viruses is still unknown and further studies are needed
to improve existing knowledge. Among the detected mutations, it is worth mentioning the
detection of the mutation PB2-E627K, an adaptive marker associated with an increased
virulence and replication in mammals, in two A(H5N1) viruses, one collected from a
domestic bird in Belgium in December 2022 and one in a wild bird in Sweden in January
2023. Moreover, about 3% of the European viruses belonging to the H5N1
A/Herring_gull/France/22P015977/2022-like genotype show mutations in the NA protein
which cause disruption of the second sialic acid binding site (2SBS), a feature typical of
human-adapted influenza A viruses (de Vries and de Haan, 2023). Among the mutations
in the HA protein which have been previously demonstrated to increase the binding to

human–type receptor, some of them (ie. S137A, S158N, T160A, S128P and R496K) have
been identified in the majority of the A(H5N1) viruses circulating in Europe since October
2022, while others (ie. T192I, S159N, Q196R, V214I) have been sporadically observed. All
the mutations associated to antiviral resistance were identified only sporadically in the
circulating viruses.
Genetic diversity of A(H5N1) viruses in mammals
Since October 2020, complete genome sequences of 57 HPAI A(H5) viruses of clade
2.3.4.4b collected from 12 distinct mammalian species (badger, cat, coati, ferret, fox, lynx,
mink, otter, polecat, porpoise and seal) in 13 European countries were generated. The
characterized viruses belong to 8 different A(H5N1) and A(H5N8) genotypes previously
identified in birds, with most of the viruses (75%) belonging to the two most widespread
genotypes in birds in Europe (H5N1 A/Eurasian_Wigeon/Netherlands/1/2020-like, H5N1
A/duck/Saratov/29-02/2021-like).
Mutations identified in A(H5N1) viruses from mammals
About half of the characterized viruses contain at least one of the adaptive markers
associated with an increased virulence and replication in mammals in the PB2 protein
(E627K, D701N or T271A) (Suttie et al., 2019). These mutations have never (T271A) or
rarely (E627K, D701N) been identified in the HPAI A(H5) viruses of clade 2.3.4.4b collected
in birds in Europe since October 2020 (<0.5% of viral sequences from birds). This
observation suggests that these mutations with potential public health implications have
likely emerged upon transmission to mammals.
Moreover, the viruses collected in October 2022 from a HPAI A(H5N1) outbreak in
intensively farmed minks in northwest Spain (Aguero et al., 2023) shows mutations in the
NA protein which cause disruption of the second sialic acid binding site (2SBS). This feature
is typical of human-adapted influenza A viruses, which may favour the emergence of
mutations in the receptor binding site of the HA protein (de Vries and de Haan, 2023).
These same mutations were detected also in seven A(H5N1) viruses from birds.
2.4 Avian influenza virus infections in humans

2.4.1 Most recent human infections with avian influenza A(H5N1)
and A(H5N6) virus
Since 3 December 2022 and as of 8 March 2023 six new human cases with avian influenza
A(H5N1) infection were reported from four countries Cambodia (2), China (2), Ecuador and
Vietnam (previously reported as A(H5) case), including two deaths (Table 4):
Ecuador for the first time reported a human infection with avian influenza A(H5N1) (clade
2.3.4.4b), marking the first human infection with A(H5N1) in South America (WHO, online-
b). The virus was detected in a 9-year old girl with severe symptoms following exposure
to sick and dead backyard poultry.
Vietnam reported for the first time since 2014, one human infection in a 5-year-old girl,
who developed severe symptoms (WHO, 2023). This case was previously reported as A(H5)
with missing neuraminidase, later confirmed as A(H5N1) virus infection with unspecified
clade but listed in WHO’s H5N1 risk assessment under clade 2.3.4.4b (WHO, 2022a). No
data are available in GISAID so far.
Two more cases, both with A(H5N1) clade 2.3.4.4b virus infection were reported in China
for the first time since 2015. Both women, 38-year and 53-year-old, developed severe
symptoms following exposure to poultry, the 38-year old woman died (WHO, 2023; BNO,
online; CHP, online)

In February 2023, Cambodia reported two cases in a family cluster involving an 11-year-
old girl (index case) and her 49-year-old father infected with A(H5N1) following exposure
to infected sick and dead backyard poultry (ECDC, 2023a, b; CDC, online-d) The girl
developed cough, sore throat and fever on 16 February 2023, was hospitalised due to
severe disease development and died on 21 February. The father of the girl developed
symptoms such as fever and cough and was isolated for several days in a referral hospital,
following A(H5N1) confirmation. All identified contacts tested negative for A(H5N1). Viral
sequencing of both specimens confirmed A(H5N1) virus clade 2.3.2.1c viruses, similar to
the viruses circulating in birds in Southeast Asia since 2014. The symptoms of both cases
occurred on the same day and both had the same exposure (sick poultry). Human-to-
human transmission has been ruled out by the local authorities.
Figure 9: Geographic distribution of human H5N1 and H5N6 cases, 2021-2023

(source: ECDC line list)
2.4.2 Human A(H5N1) cases, summary

As of 3 March 2023, there have been 873 cases, including 458 deaths of human infection
with avian influenza A(H5N1) reported from 22 countries (Azerbaijan, Bangladesh,
Cambodia, Canada, China, Djibouti, Ecuador, Egypt, Indonesia, India, Iraq, Laos,
Myanmar, Nepal, Nigeria, Pakistan, Spain, Thailand, Türkiye, Vietnam, United Kingdom
and United States).

2022: China (1), Spain (2), United States of America (1), Vietnam (1)
2023: Cambodia (2), China (1), Ecuador (1)
Figure 10: Distribution of confirmed human cases of avian influenza A(H5N1)

virus infection by year of onset and country, 2003–2023 (updated on 2
March 2023, n=873)
2.4.3 Human A(H5N6) cases, summary

As of 3 March 2023, China (83) and Laos (1) reported a total of 84 human infections with
avian influenza A(H5N6) including 29 (35%) with fatal outcome. Since 2021, A(H5N6)
viruses cluster also in clade 2.3.4.4b although sequence information is only available for a
minority of viruses.

Figure 11: Distribution of confirmed human cases of avian influenza A(H5N6)

virus infection by year of onset and country, 2014–2023 (updated on 2
March 2023, n=84)
2.4.4 Details about human infections with avian influenza A(H5Nx)

virus clade 2.3.4.4b related to viruses circulating in Europe,
2021–2023
In October 2022, Spanish authorities reported two workers involved in culling and cleaning
activities to have tested positive for A(H5N1). However, due to low virus load no full
genome could be generated and no seroconversion was present in the workers. This
indicates rather a contamination of the mucosa with avian influenza viruses due to
exposure to highly contaminated environment despite wearing personal protective
equipment (PPE) and not a systemic infection (Aznar et al., 2023) (ECDC, 2022a, b;
Sanidad, 2022; WHO, online-a). Other farm workers involved in the culling activities during
the outbreak at the same farm tested negative. Close contacts were followed up and all
tested negative, providing evidence that there was no human-to-human transmission.
Spanish authorities consider these findings the result of an environmental contamination
and not an active replication of the virus in the human hosts. This is also reflected in the
low virus load in the tested specimens resulting in high Ct values in the initial PCR tests at
the detection limit of the assay, the inability to generate full length genomes, the lack of
virus cultivation and inconclusive or negative serological findings (Table 3).
In a mink farm an outbreak of H5N1 was identified following increased mortality in the
animals (Aguero et al., 2023). All workers on this farm were wearing PPE and tested
negative for influenza.
Earlier human infections with A(H5N1) or A(H5N8) viruses of clade 2.3.4.4b were reported
since 2021, in the US, the United Kingdom, Russia and Nigeria, all related to outbreaks in
poultry or wild birds (Pyankova et al., 2021; WHO, 2021b; CDC, online-b). So far,
information from some of these human A(H5) cases suggested PCR amplification of low-
level virus RNA following exposure to contaminated environment and infected birds during

culling activities and no active viral replication in infected human cells or tissues with lack
of seroconversion (Table 3).
Sequence data from A(H5N1) viruses detected in China in birds and shared through GISAID
have shown that the HA genes of the viruses belong to clade 2.3.4.4b and cluster with
viruses collected in Europe, Africa and other Asian countries since 2020, however, the other
gene segments indicate a high genetic variability among the circulating viruses in China
and differ in at least one gene segment from European viruses.
H5Nx detections in human reported as asymptomatic or with mild symptoms are mostly
related to male workers involved in culling activities and wearing personal protective
equipment (PPE) (Table 3). Recent human cases reported with severe or fatal outcome
have all been women exposed without personal protective equipment to sick or dead
backyards poultry (Table 4). This indicates the increased risk associated with backyard
settings and with unprotected exposure to infected birds likely due to lack of knowledge or
awareness of the risk of avian influenza for human health.
Table 3: Human cases due to clade 2.3.4.4b viruses – asymptomatic cases
Date Country Case(s) Exposure Symptom Confirmation

reported (subtype)
Sept/Oct Spain 19-year Culling Asymptomatic PCR, partial

2022 (H5N1) male (PPE) sequencing, no culture,
(27 27-year no serological reactivity
Sept/13 male against H5
Oct)
Apr 2022 USA (H5N1) 18+ Culling Fatigue PCR, partial sequence
(20 April) male (PPE) data, no virus isolation
possible
Jan 2022 UK (H5N1) 80+ Raised Asymptomatic PCR, reproduced on

(24 Dec male birds, two successive swabs
2021) “lived following days high Ct
with” values
Apr 2021 Nigeria (H5 3 (7) Culling Asymptomatic 7 type A positive, 3 H5

related to positive PCR, no full
H5N1 sequencing or culture
outbreak)
Feb 2021 Russia 7 Culling Asymptomatic 7 PCR, 1 isolated, 4 pos

(H5N8) (PPE) focus reduction
neutralisation assay
(FRNA) serum titres, 1
4-fold in sample 14d
after (1:20), decreased
titre 44d after; 5
samples positive for
IgG biolayer
interferometry
Source: (Pyankova et al., 2021; WHO, 2021a, c; Oliver et al., 2022; WHO, 2022b; Aznar et al., 2023; CDC,
online-c; ECDC, online; WHO, online-c)

Table 4: Human cases due to clade 2.3.4.4b viruses – symptomatic cases
Date Country Case(s) Exposure Symptoms Confirmation

reported (subtype)
(symptom
onset)
14 Oct 2022 China 38-year Backyard Hospitalised Low concentration of virus,

(22 Sept) (H5N1) woman poultry with severe only partial sequences of
pneumonia, eight segments all avian
died 18 Oct influenza virus origin.
Sequence of HA belonged
to Clade 2.3.4.4b, and
clustered with Asian
viruses, not European
viruses.
The receptor binding site
not determined. PB2: 591Q
and 627E low reads).
9 Jan 2023 Ecuador 9-year Backyard Conjunctival PCR with high Ct values, no
(25 Dec (H5N1) girl poultry pruritus, NA-typing, partial sequence
2022) sick/dead coryza, data available
nausea,
vomiting,
constipation,
meningitis,
admitted to
hospital and
ICU with
pneumonia
and septic
shock,
mechanical
ventilation
1 Mar 2023 China 53-year Exposure Symptomatic, Sequence data available

(31 Jan) (H5N1) woman to poultry no details
available
Source: (WHO, 2022a, b; ECDC, 2023a; OPS, 2023; WHO, 2023; BNO, online; WHO, online-b)
2.4.5 Genetic characteristics of HPAI viruses of the A(H5NX) subtype

from human
Based on the data available from the GISAID EpiFlu database, since 2020 human infections
have been caused by four different A(H5) clades of the A/goose/Guangdong/1/1996-
lineage, namely 2.3.2.1c (Laos, 2020 and Cambodia, 2023), 2.3.2.1a (India, 2021),
2.3.4.4h (China, 2020-2021), 2.3.4.4b (China, Europe, North and South America).
Mutation Q226L was identified in two A(H5N6) viruses of clade 2.3.4.4b collected in China
in 2021 (Zhu W Fau - Li et al.)to the switch in the receptor specificity from avian-type to
human-type receptor (Stevens et al., 2006; Chutinimitkul et al.; Russell et al., 2012). This
mutation was previously detected in two A(H5N1) viruses of clade 1 collected from human
infections in Cambodia in 2013 (Rith et al., 2014) and, based on the available sequence
data, it is not present in the clade 2.3.4.4b A(H5Nx) viruses currently circulating in the
avian population in Europe. Moreover, six clade 2.3.4.4b A(H5N6) viruses collected from
human infections in China in 2021 possessed one of the adaptive markers in the PB2
protein (Q591K, E627K or D701N) associated with an increased virulence and replication
in mammals (Zhu W Fau - Li et al., 2022)

2.4.6 Additional information and international risk assessments

A study on currently circulating A(H5N1) viruses in North America showed that these
viruses are able to replicate efficiently in human respiratory tract cell types and that in
ferret infection and transmission studies, animals got infected but showed only very mild
symptoms mostly limited to upper respiratory tract and viruses did not transmit to other
ferrets kept in a direct-contact setting (Pulit-Penaloza et al., 2022).
The previously issued risk assessment using the Influenza Risk Assessment Tool (IRAT) of
the United States Centers for Disease Control and Prevention (US CDC) placed the risk of
clade 2.3.4.4b viruses in the lower moderate category (CDC, 2021). The risk of the
A(H5N1) clade 2.3.4.4b viruses currently circulating in the United States bird and poultry
populations, and which are closely related to European viruses, were assessed by the US
CDC to be of low risk for human health in the general population and higher for people
occupationally or recreationally exposed to birds (CDC, online-a, c) . The WHO assessed
the risk related to the recent (H5N1) human cases as low for the general public and low to
moderate for occupationally exposed people (WHO, 2022a, online-a). WHO previously
assessed the risk for A(H5N6) that “the zoonotic threat remains elevated due to spread of
the viruses in birds, based on evidence available so far, the overall pandemic risk is
considered not significantly changed in comparison to previous years” (WHO, 2021d). The
UKHSA assesses that ‘at present there are ‘no indicators of increasing risk to human health
with a low confidence’ (GovUK, online). A joint EFSA, ECDC, EURL publication from 2021
already described the threat to humans with the objective to raise awareness among
clinicians in the EU around zoonotic avian influenza virus infection and consider testing
(Adlhoch et al., 2021).
2.5 ECDC risk assessment for the general public in the EU/EEA
Sporadic human cases of different avian influenza A(H5Nx) subtypes have been previously
reported globally and current epidemiological and virological evidence suggests that
A(H5N1) viruses remain avian-like. Mutations associated with mammalian adaptation such
as in the PB2 that confer an increased replication have been observed, however, no
mutations in the Hemagglutinin (HA) gene have been detected in A(H5N1) viruses from
birds or mammals that would support a switch of the viruses from avian-like alpha2.3 to
human-like alpha 2.6sialic acid receptors (Shinya and Kawaoka, 2006; de Graaf and
Fouchier, 2014).
Despite the high number of exposure events due to the large outbreaks in poultry and wild
birds over the last three years, no symptomatic human infection due to avian influenza
A(H5Nx) have been reported from EU/EEA countries. Only sporadic human infections have
been reported globally, and transmission to humans remains a rare event. No sustained
transmission between humans has been observed.
Currently developed and proposed Candidate Vaccine Viruses (CVVs) for pandemic
preparedness by WHO have been assessed to be antigenically similar to currently
circulating viruses in Europe and a more US-virus related new CVV has been proposed
(WHO, 2022a, 2023).
ECDC published a Threat Assessment Brief in February 2021 that assessed the risk as very
low for the general population and low for occupationally exposed people (ECDC, 2021b)
and revised the risk to low for the general population and low to moderate for
occupationally exposed people in December 2021 due to the increase in transmission
events to mammal species including sporadic human cases with no or mild symptoms. The
assessment remains valid.
Overall, the risk of infection with avian influenza viruses of the currently circulating clade
2.3.4.4b in Europe for the general public in EU/EEA countries is considered to be low. The
risk to occupationally or otherwise exposed groups to avian influenza infected birds or
mammals such as cullers or veterinarians has been assessed as low to moderate.

The high diversity and ongoing reassortment events globally also after the introduction
into the Americas add a high uncertainty to the assessment, and sporadic transmission
events to humans causing also severe infections cannot be excluded.
Avian influenza virus transmission to humans is a rare event, viruses remain avian-like
adapted. Mutations in the HA gene have been identified from in vitro studies associated
with increased binding to human-type receptor. However, the viruses do not show the key
mutations in the receptor binding domain that cause the switch from avian to human type
receptors and do not possess all the mutations that have been shown in gain of function
studies to be determinant for H5 droplet respiratory transmission in ferrets (Herfst et al.,
2012; Imai et al., 2012). However, detections of Q226L mutation in the HA gene in two
human cases with A(H5N6) in 2021 in China are important indicators that need to be
considered relevant, but these mutations seem to be isolated and have not been described
in any recent human A(H5N1) cases and any other human avian influenza case since 2021
(Zhu W Fau - Li et al., 2022). WHO also assessed these findings as isolated and ‘molecular
markers were not identified in viruses collected from environmental surfaces or poultry
indicating that these amino acid substitutions occurred sporadically during human infection’
(WHO, 2021d).
However, the expansion of mammal species identified infected with A(H5N1) viruses as
well as the detection of viruses carrying markers for mammalian adaptation in other genes
such as the PB2 that correlated with increased replication and virulence in mammals, is of
concern. The additional reports of transmission events to and potentially between
mammals, e.g. mink, sea lion, seals, foxes and other carnivores as well as
seroepidemiological evidence of transmission to wild boar and domestic pigs, associated
with evolutionary processes including mammalian adaptation are of concern and need to
be closely followed up.
With the wide geographical distribution of avian influenza viruses and high number of
detections also in wild birds and mammals, sporadic human cases infected with HPAI
viruses cannot be ruled out whenever people are exposed to infected sick or dead birds.
The likelihood of travel-related importation of human avian influenza cases from countries
where the viruses are detected in poultry or wild birds is considered to be very low.
The uncertainty of this risk assessment is high due to the high variability and diversification
of the avian influenza viruses of clade 2.3.4.4 with many reassorted subtypes and genetic
lineages co-circulating in Europe and globally. Reassortment events will continue and
zoonotic transmission of avian influenza viruses cannot be fully excluded in general when
avian influenza viruses are present in birds.
2.6 Options for public health response

Direct contact with infected birds or a contaminated environment is the most likely source
of infection. The use of personal protective equipment for people exposed to dead birds or
their droppings is recommended to minimise the risk of infection. Detailed information on
occupational safety and health in the work place has been provided in the last report (EFSA
et al., 2022).
The recent severe cases in Asia and South America in individuals exposed to infected sick
and dead backyard poultry underline the risk associated with unprotected contact with
infected birds.
People should avoid touching sick or dead birds or their droppings and should wear personal
protective equipment (PPE) when in direct contact. In general, sick and dead wild mammals
should not be touched without proper precautionary measures such as PPE. Workers should
be protected following an updated workplace risk assessment and preventive measures
should be set accordingly10. Active or passive follow-up measures should be in place for

people exposed to potentially infected birds (and mammals) for 10-14 days. Testing should
be initiated immediately for symptomatic people and contact people of confirmed cases.
ECDC jointly with EFSA, EU-OSHA and the EURL published a separate document that
provides guidance for the testing of humans for zoonotic influenza viruses. The document
describes different exposed groups at risk and raises awareness about the possibility of
atypical presentations in humans similar to what has been recently observed in other
mammals with severe infection of the brain, i.e. encephalitis or meningoencephalitis
(ECDC, 2022d).
A guidance document on integrated surveillance of respiratory viruses has been published

in 2022 that is also relevant for zoonotic incl avian influenza virus infections in humans
(ECDC, 2022c). Primary and secondary health care sentinel systems as well as molecular
surveillance have been strengthened during the COVID-19 pandemic to integrate
respiratory viruses as well as e.g. monitor the emergence of SARS-CoV-2 variants and will
be useful for any other emerging respiratory viruses. Surveillance and options for public
health measures have been outlined in previous reports (EFSA et al., 2021b) and remain
valid.
Human infections with avian influenza viruses are notifiable under EU legislation within 24
hours through the Early Warning and Response System (EWRS) according to EU Decision
1082/2013/EU9. Reporting is also required through the International Health Regulations
(IHR) notification system (WHO, 2017).
A guidance on infection prevention and control measures in health care in regard to

respiratory viruses has been updated and includes also high threat pathogens (ECDC,
2021a).
The use of antiviral pre- and postexposure should be considered for exposed people and
in particular for possible cases of avian influenza infection according to national guidelines.
Candidate vaccine viruses (CVV) developed, under development or proposed are listed at
WHO (WHO, 2021b). A new CVV for H5 viruses more antigenically like a new clade 2.3.4.4b
CVV that is antigenically like A/American wigeon/South Carolina/22-000345-001/2021 has
been proposed during the Vaccine Composition Meeting for the Northern Hemisphere in
February 2023 more similar to recently circulating avian influenza H5 viruses in the US
(WHO, 2023).

3 Conclusions
Birds in Europe:
• During the current reporting period, from 3 December to 1 March, an unexpected

increased detection of HPAI A(H5N1) virus was reported in gull species, particularly
in black headed gulls linked to mortality events in France, Belgium, the Netherlands,
Italy.
• Genetic analysis based on the available data support the hypothesis that HPAI
viruses persisted in Europe in residential wild bird populations during and after the
summer months as no new virus introductions were identified; the increased
genetic diversity observed since autumn 2022 has very likely emerged from
reassortment events with avian influenza viruses circulating in Eurasian wild bird
populations.
• The viruses which have been badly affecting the black-headed gulls in The
Netherlands, Belgium, France and Italy since December 2022 are closely related
and belong to the genotype H5N1 A/Herring_gull/France/22P015977/2022-like.
This genotype had emerged during the summer in Europe through reassortment
events with the gull-adapted H13 subtype and have mainly been detected in gulls.
The behavior of this genotype in poultry species will have to be studied in the
coming months
• The A(H5N1) viruses currently circulating in Europe retain a preferential binding for
avian-like receptors; however, several mutations associated to increased zoonotic
potential have been detected. AllTheir effects on the biological characteristics of the
viruses are not fully unknown.
• As for poultry, whilst most outbreaks have been identified as primary
introductions (likely from infected wild birds), secondary spread in both poultry
and captive birds has taken place. Regardless of the source of infection, primary
introduction or secondary spread, high levels of biosecurity measures and prompt
reporting of suspicions need to be kept in order to minimize the risk of infection
and further transmission.
• From October 2020 to date, the trend in the numbers of outbreaks in poultry
correlates mainly with the trend in the number of detections in waterfowl. Increased
detections in seabirds, during the summer months of 2022 were in contrast with
the lower number of detections in poultry. However, detections in those summer
months involved mostly herring gulls on coastal locations, whilst detections during
the current reporting period extended inland and involved mostly black headed
gulls.
• The sustained circulation of HPAI virus in black headed gull and other gull species,
during the last winter weeks and the coming spring/summer months, might increase
the risk of infection for poultry as breeding colonies spread mostly inlands possibly
overlapping with poultry production areas.
Birds outside Europe:
• In the current reporting period from 3 December 2022 to 1 March 2023 the HPAI
(H5N1) virus continued to spread in South America, from Mexico to Chile to the
furthest south that the virus has reached (latitude: 42 degrees South), near to the
southern tip of South America.
• Based on the observed temporal and geographical distribution of HPAI (H5N1) in

wild birds during the reporting period, virus spread in South America corresponds
to the Pacific Americas Flyway along the west coast of South America, the
Mississippi Flyway along the Caribbean and the north-central part of South America,
and the Atlantic Americas Flyway along the east coast of South America.
• Given the rapid southwards spread of HPAI A(H5N1) virus, and the known
movements of wild birds between South America and the Antarctic, e.g. sheathbills

(Mead CJ and Richford AS, 2003), there is risk of virus spread to seabirds (100
million breeding birds) and pinnipeds (seven pinniped species, including 15 million
crabeater seals) of the Antarctic9
• The results of the genetic analysis conducted on HPAI viruses isolated from South
America indicate multiple virus introductions events from North to South America,
followed by local spread.
• The spread of HPAI virus in South America has also reached domestic birds, with
the majority of the reported outbreaks involving captive (backyard) birds. Backyard
keeping of poultry is done with low levels of biosecurity and may represent a public
health risk, as exemplified by infection of a girl in Ecuador. In addition, depending
on the production and commercial structure of poultry in those countries, backyard
may also represent a source of infection for commercial farms. New outbreaks in
domestic birds are being reported, which indicates that the epidemiological situation
in this region is still evolving.
Mammals:
• During this reporting period the reports of HPAI (H5N1) virus in individual
mammals, mainly carnivores, that were likely infected through feeding on infected
wild birds continued.
• In addition to the mass mortality events in mammals due to HPAI (H5N1) observed
in free-living harbour seals in the USA in summer 2022 and in American mink in
Spain in autumn 2022, in this reporting period there was a mass mortality of South
American sea lions associated to HPAI A(H5N1) virus in Peru in January and
February 2023. In all three events, there may have been mammal-to-mammal
transmission of HPAI A(H5N1) virus. A(H5) infections in mammalian species appear
to favour the emergence of molecular markers of virus adaptation to mammals (ie.
PB2 E627K, D701N or T271A).
Human cases:
• Sporadic human infections with avian influenza viruses of different H5 clades are
reported from different countries globally
• Human infections are related to unprotected exposure to sick and dead poultry
particularly in backyard settings also causing severe disease and fatal outcome
4 Options for response

In birds:
• It is important to accurately report infected wild birds—including identification of

species—and the associated mortality and, where appropriate, to remove wild bird
carcasses from affected sites to limit virus spread. The benefits of wild bird carcass
removal—reduction of virus load—need to be weighed up against the possible
disturbance of wildlife.
• Considering the high negative impact of HPAI A(H5) epidemics in the last years,
short-term preparedness and medium- and long-term prevention strategies should
be identified and implemented, primarily in densely populated poultry areas and
poultry production systems that are highly susceptible to avian influenza exposure.
These were described in detail in Avian influenza overview September – December
2021 (EFSA, 2021) and in 2022 EFSA Avian influenza Quarterly Reports.
9
https://en.wikipedia.org/wiki/Southern_Ocean#cite_note-FOOTNOTE''EB''1878-1

In mammals:
• Extended and enhanced surveillance of both wild mammals (particularly carnivores)

and farmed mammals (particularly American mink and domestic pigs) in risk areas
where HPAI is present in wild birds and poultry is recommended.
• Improve virological and serological surveillance in scavenger mammals to prompt
identify viruses with zoonotic potential and evaluate the real magnitude of the
spread of HPAI viruses in these species.
• In domestic mammals, to prevent exposure to possible infected wild birds by
increasing biosecurity at farm.
• Timely producing and sharing viral sequences, which should be analysed in real-
time to assess the pandemic risk.
• Better, more accurate and timely reporting of HPAI virus detections in mammals in
a way that reliable numbers of infected animals could be used as quantitative
information for risk assessment.
• Thoroughly investigate the dynamic of the infection in case of mass mortality events
associated with HPAI virus detected in mammalian species. Testing a high number
of animals and assuring a prompt generation and sharing of viral sequences data
are of utmost importance to shed light on the virus origin, evolution and possible
transmission between individuals.
In humans:
• Appropriate use of personal protective equipment when in contact with potentially

infected birds and animals.
• Follow-up exposed people (also to infected mammals), test and identify
transmission events early.
• Suspicion and detection of human infection with avian influenza should be identified
and reported as early as possible.
• Antiviral pre-and post-exposure prophylaxis should be considered following national
guidelines.
• Timely producing and sharing of virus sequence information is crucial for
assessment and development of candidate vaccine viruses.
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Annex A – Data on birds

The Annex contains tables and figures on wild birds species and movements and HPAI virus
detections in birds.
The annex is available on the EFSA Knowledge Junction community on Zenodo at:
https://doi.org/10.5281/zenodo.7707605

Avian Influenza Overview March 2023

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SCIENTIFIC REPORT

APPROVED: 8 March 2023

Avian influenza overview December 2022 – March

Requestor: European Commission

Question number: EFSA-Q-2023-00094 and Commission request 280 to ECDC

Correspondence: biohaw@efsa.europa.eu and ECDC.influenza@ecdc.europa.eu

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The EFSA Journal is a publication of the European Food

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2.2 HPAI detections in mammals 16

2.3 Genetic characterisation of avian influenza viruses 21

2.4 Avian influenza virus infections in humans 23

2.6 Options for public health response 30

Annex A – Data on birds 43

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Although categorized under 'colony-breeding seabirds’ in EFSA reports, black-headed gulls

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Figure 2: Geographical distribution, based on available geocoordinates, of highly

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Figure 3: Distribution of the highly pathogenic avian influenza virus detections in

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Figure 4: Distribution of total number of HPAI virus detections reported in Europe

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Figure 5: Geographical distribution, based on available geocoordinates, of highly

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Figure 6: Geographical distribution, based on available geocoordinates, of highly

In Central America (Guatemala, Honduras, El Salvador, Nicaragua, Costa Rica, Panama),

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Table 1: Number of HPAI virus detections in non-European countries, by virus subtype

Domestic birds Wild birds

Source: WOAH-WAHIS (data extraction carried out on 1 March 2023).

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Figure 7: Geographical distribution, based on available geocoordinates, of highly

2.2 HPAI detections in mammals

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Virus Animal (order, family, species) Epidemic

France (Herve et al., 2021)

Ferret (Mustela furo) Slovenia, Belgium

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Mountain lion (Puma concolor) USA 2022-2023 (WOAH, online-b)

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2.3 Genetic characterisation of avian influenza viruses

2.3.2 Global overview of HPAI viruses of the A(H5) subtype of clade

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2.3.3 Genetic characteristics of HPAI viruses of the A(H5N1) subtype

Since October 2020, 6 subtypes (A(H5N1), A(H5N2), A(H5N3), A(H5N4), A(H5N5),

Genotype H5N1 A/Herring_gull/France/22P015977/2022-like had emerged through

Mutations identified in A(H5N1) viruses from avian species

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Genetic diversity of A(H5N1) viruses in mammals

Mutations identified in A(H5N1) viruses from mammals

2.4 Avian influenza virus infections in humans

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Figure 9: Geographic distribution of human H5N1 and H5N6 cases, 2021-2023

2.4.2 Human A(H5N1) cases, summary

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